XB-ART-40657
Dev Biol
January 15, 2010;
337
(2):
335-50.
BMP antagonists and FGF signaling contribute to different domains of the neural plate in Xenopus.
Abstract
In ectodermal explants from Xenopus embryos, inhibition of BMP signaling is sufficient for neural induction, leading to the idea that neural fate is the default state in the ectoderm. Many of these experiments assayed the action of BMP antagonists on animal caps, which are relatively naïve explants of prospective ectoderm, and different results have led to debate regarding both the mechanism of neural induction and the appropriateness of animal caps as an assay system. Here we address whether BMP antagonists are only able to induce neural fates in pre-patterned explants, and the extent to which neural induction requires FGF signaling. We suggest that some discrepancies in conclusion depend on the interpretations of sox gene expression, which we show not only marks definitive neural tissue, but also tissue that is not yet committed to neural fates. Part of the early sox2 domain requires FGF signaling, but in the absence of organizer signaling, this domain reverts to epidermal fates. We also reinforce the evidence that ectodermal explants are naïve, and that explants that lack any dorsal prepattern are readily neuralized by BMP antagonists, even when FGF signaling is inhibited.
PubMed ID: 19913009
PMC ID: PMC2812634
Article link: Dev Biol
Grant support: [+]
GM49346 NIGMS NIH HHS , R01 GM049346-17A1 NIGMS NIH HHS , R01 GM049346 NIGMS NIH HHS , T32 GM007232 NIGMS NIH HHS
Species referenced: Xenopus laevis
Genes referenced: chrd.1 egr2 en2 fgf8 fst gsc hes4 hoxb9 hoxc9-like krt12.4 mos ncam1 nkx2-1 nog nrp1 odc1 otx2 pax3 snai2 sox2 sox3 tbxt tubb2b zic2
Morpholinos: chrd.1 MO1 chrd.1 MO2 ctnnb1 MO1 fst MO1 nog MO1
Article Images: [+] show captions
References [+] :
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Bachiller,
The organizer factors Chordin and Noggin are required for mouse forebrain development.
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Pubmed
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Fuentealba, Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. 2007, Pubmed , Xenbase
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Hensey, Programmed cell death during Xenopus development: a spatio-temporal analysis. 1998, Pubmed , Xenbase
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Oelgeschläger, Chordin is required for the Spemann organizer transplantation phenomenon in Xenopus embryos. 2003, Pubmed , Xenbase
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Rossant, Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. 2009, Pubmed
Sapkota, Balancing BMP signaling through integrated inputs into the Smad1 linker. 2007, Pubmed , Xenbase
Sasai, Endoderm induction by the organizer-secreted factors chordin and noggin in Xenopus animal caps. 1997, Pubmed , Xenbase
Sharpe, A homeobox-containing marker of posterior neural differentiation shows the importance of predetermination in neural induction. 1987, Pubmed , Xenbase
Sokol, Pre-existent pattern in Xenopus animal pole cells revealed by induction with activin. 1991, Pubmed , Xenbase
Stewart, The anterior extent of dorsal development of the Xenopus embryonic axis depends on the quantity of organizer in the late blastula. 1990, Pubmed , Xenbase
Streit, Initiation of neural induction by FGF signalling before gastrulation. 2000, Pubmed
Streit, Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo. 1998, Pubmed
Uzgare, Mitogen-activated protein kinase and neural specification in Xenopus. 1999, Pubmed , Xenbase
Varga, Chordin expression, mediated by Nodal and FGF signaling, is restricted by redundant function of two beta-catenins in the zebrafish embryo. 2007, Pubmed
Wawersik, Conditional BMP inhibition in Xenopus reveals stage-specific roles for BMPs in neural and neural crest induction. 2004, Pubmed , Xenbase
Wegner, From stem cells to neurons and glia: a Soxist's view of neural development. 2005, Pubmed
Wills, Twisted gastrulation is required for forebrain specification and cooperates with Chordin to inhibit BMP signaling during X. tropicalis gastrulation. 2005, Pubmed , Xenbase
Wilson, Induction of epidermis and inhibition of neural fate by Bmp-4. 1995, Pubmed , Xenbase
Xanthos, The roles of three signaling pathways in the formation and function of the Spemann Organizer. 2002, Pubmed , Xenbase
Zhu, Regulation of acetylcholinesterase expression by calcium signaling during calcium ionophore A23187- and thapsigargin-induced apoptosis. 2006, Pubmed
Barnett, Neural induction and patterning by fibroblast growth factor, notochord and somite tissue in Xenopus. 1998, Pubmed , Xenbase
Bolce, Ventral ectoderm of Xenopus forms neural tissue, including hindbrain, in response to activin. 1992, Pubmed , Xenbase
Chang, Neural induction requires continued suppression of both Smad1 and Smad2 signals during gastrulation. 2007, Pubmed , Xenbase
Christen, FGF-8 is associated with anteroposterior patterning and limb regeneration in Xenopus. 1998, Pubmed , Xenbase
Cox, Caudalization of neural fate by tissue recombination and bFGF. 1996, Pubmed , Xenbase
Delaune, Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition. 2004, Pubmed , Xenbase
Fletcher, FGF8 spliceforms mediate early mesoderm and posterior neural tissue formation in Xenopus. 2006, Pubmed , Xenbase
Fletcher, The role of FGF signaling in the establishment and maintenance of mesodermal gene expression in Xenopus. 2008, Pubmed , Xenbase
Fuentealba, Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. 2007, Pubmed , Xenbase
Gerhart, Region-specific cell activities in amphibian gastrulation. 1987, Pubmed , Xenbase
Gerhart, Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development. 1990, Pubmed , Xenbase
Gimlich, Acquisition of developmental autonomy in the equatorial region of the Xenopus embryo. 1986, Pubmed , Xenbase
Green, Roads to neuralness: embryonic neural induction as derepression of a default state. 1994, Pubmed , Xenbase
Grunz, Neural differentiation of Xenopus laevis ectoderm takes place after disaggregation and delayed reaggregation without inducer. 1990, Pubmed , Xenbase
Heasman, Beta-catenin signaling activity dissected in the early Xenopus embryo: a novel antisense approach. 2000, Pubmed , Xenbase
Hemmati-Brivanlou, Vertebrate neural induction. 1997, Pubmed , Xenbase
Hensey, Programmed cell death during Xenopus development: a spatio-temporal analysis. 1998, Pubmed , Xenbase
Kengaku, bFGF as a possible morphogen for the anteroposterior axis of the central nervous system in Xenopus. 1995, Pubmed , Xenbase
Khokha, Techniques and probes for the study of Xenopus tropicalis development. 2002, Pubmed , Xenbase
Khokha, Depletion of three BMP antagonists from Spemann's organizer leads to a catastrophic loss of dorsal structures. 2005, Pubmed , Xenbase
Kim, Expression of the BMP antagonist Dan during murine forebrain development. 2003, Pubmed
Kim, XATH-1, a vertebrate homolog of Drosophila atonal, induces a neuronal differentiation within ectodermal progenitors. 1997, Pubmed , Xenbase
Kintner, Expression of Xenopus N-CAM RNA in ectoderm is an early response to neural induction. 1987, Pubmed , Xenbase
Knecht, Dorsal-ventral patterning and differentiation of noggin-induced neural tissue in the absence of mesoderm. 1995, Pubmed , Xenbase
Kudoh, Combinatorial Fgf and Bmp signalling patterns the gastrula ectoderm into prospective neural and epidermal domains. 2004, Pubmed
Kuroda, Neural induction in Xenopus: requirement for ectodermal and endomesodermal signals via Chordin, Noggin, beta-Catenin, and Cerberus. 2004, Pubmed , Xenbase
Lamb, Neural induction by the secreted polypeptide noggin. 1993, Pubmed , Xenbase
Lamb, Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior neural pattern. 1996, Pubmed , Xenbase
Launay, A truncated FGF receptor blocks neural induction by endogenous Xenopus inducers. 1996, Pubmed , Xenbase
Linker, Cell communication with the neural plate is required for induction of neural markers by BMP inhibition: evidence for homeogenetic induction and implications for Xenopus animal cap and chick explant assays. 2009, Pubmed , Xenbase
Linker, Neural induction requires BMP inhibition only as a late step, and involves signals other than FGF and Wnt antagonists. 2004, Pubmed , Xenbase
Liu, Inhibition of neurogenesis by SRp38, a neuroD-regulated RNA-binding protein. 2005, Pubmed , Xenbase
Maegawa, FGF signaling is required for {beta}-catenin-mediated induction of the zebrafish organizer. 2006, Pubmed
McGrew, Wnt and FGF pathways cooperatively pattern anteroposterior neural ectoderm in Xenopus. 1998, Pubmed , Xenbase
Oelgeschläger, Chordin is required for the Spemann organizer transplantation phenomenon in Xenopus embryos. 2003, Pubmed , Xenbase
Papanayotou, A mechanism regulating the onset of Sox2 expression in the embryonic neural plate. 2008, Pubmed
Pera, Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction. 2003, Pubmed , Xenbase
Rentzsch, Fgf signaling induces posterior neuroectoderm independently of Bmp signaling inhibition. 2004, Pubmed
Reversade, Depletion of Bmp2, Bmp4, Bmp7 and Spemann organizer signals induces massive brain formation in Xenopus embryos. 2005, Pubmed , Xenbase
Reversade, Regulation of ADMP and BMP2/4/7 at opposite embryonic poles generates a self-regulating morphogenetic field. 2005, Pubmed , Xenbase
Ribisi, Ras-mediated FGF signaling is required for the formation of posterior but not anterior neural tissue in Xenopus laevis. 2000, Pubmed , Xenbase
Richter, Gene expression in the embryonic nervous system of Xenopus laevis. 1988, Pubmed , Xenbase
Richter, A developmentally regulated, nervous system-specific gene in Xenopus encodes a putative RNA-binding protein. 1991, Pubmed , Xenbase
Rossant, Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. 2009, Pubmed
Sapkota, Balancing BMP signaling through integrated inputs into the Smad1 linker. 2007, Pubmed , Xenbase
Sasai, Endoderm induction by the organizer-secreted factors chordin and noggin in Xenopus animal caps. 1997, Pubmed , Xenbase
Sharpe, A homeobox-containing marker of posterior neural differentiation shows the importance of predetermination in neural induction. 1987, Pubmed , Xenbase
Sokol, Pre-existent pattern in Xenopus animal pole cells revealed by induction with activin. 1991, Pubmed , Xenbase
Stewart, The anterior extent of dorsal development of the Xenopus embryonic axis depends on the quantity of organizer in the late blastula. 1990, Pubmed , Xenbase
Streit, Initiation of neural induction by FGF signalling before gastrulation. 2000, Pubmed
Streit, Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo. 1998, Pubmed
Uzgare, Mitogen-activated protein kinase and neural specification in Xenopus. 1999, Pubmed , Xenbase
Varga, Chordin expression, mediated by Nodal and FGF signaling, is restricted by redundant function of two beta-catenins in the zebrafish embryo. 2007, Pubmed
Wawersik, Conditional BMP inhibition in Xenopus reveals stage-specific roles for BMPs in neural and neural crest induction. 2004, Pubmed , Xenbase
Wegner, From stem cells to neurons and glia: a Soxist's view of neural development. 2005, Pubmed
Wills, Twisted gastrulation is required for forebrain specification and cooperates with Chordin to inhibit BMP signaling during X. tropicalis gastrulation. 2005, Pubmed , Xenbase
Wilson, Induction of epidermis and inhibition of neural fate by Bmp-4. 1995, Pubmed , Xenbase
Xanthos, The roles of three signaling pathways in the formation and function of the Spemann Organizer. 2002, Pubmed , Xenbase
Zhu, Regulation of acetylcholinesterase expression by calcium signaling during calcium ionophore A23187- and thapsigargin-induced apoptosis. 2006, Pubmed